Organelles that illuminate the origins of trichomonas hydrogenosomes and giardia mitosomes

ABSTRACT Many anaerobic microbial parasites possess highly modified mitochondria known as mitochondrion-related organelles (MROs). The best-studied of these are the hydrogenosomes of

_Trichomonas vaginalis_ and _Spironucleus salmonicida_, which produce ATP anaerobically through substrate-level phosphorylation with concomitant hydrogen production; and the mitosomes of

_Giardia intestinalis_, which are functionally reduced and lack any role in ATP production. However, to understand the metabolic specializations that these MROs underwent in adaptation to

parasitism, data from their free-living relatives are needed. Here, we present a large-scale comparative transcriptomic study of MROs across a major eukaryotic group, Metamonada, examining

lineage-specific gain and loss of metabolic functions in the MROs of _Trichomonas_, _Giardia_, _Spironucleus_ and their free-living relatives. Our analyses uncover a complex history of ATP

production machinery in diplomonads such as _Giardia_, and their closest relative, _Dysnectes_; and a correlation between the glycine cleavage machinery and lifestyles. Our data further

suggest the existence of a previously undescribed biochemical class of MRO that generates hydrogen but is incapable of ATP synthesis. Access through your institution Buy or subscribe This is

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GENERATES ENERGY FOR CILIATE HOST BY DENITRIFICATION Article Open access 03 March 2021 THE TERRESTRIAL ISOPOD SYMBIONT ‘_CANDIDATUS_ HEPATINCOLA PORCELLIONUM’ IS A POTENTIAL NUTRIENT

SCAVENGER RELATED TO _HOLOSPORALES_ SYMBIONTS OF PROTISTS Article Open access 08 March 2023 EXTREME MITOCHONDRIAL REDUCTION IN A NOVEL GROUP OF FREE-LIVING METAMONADS Article Open access 09

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PubMed  PubMed Central  Google Scholar  Download references ACKNOWLEDGEMENTS M.K., M.M.L. and C.W.S. were supported by a grant (MOP-142349) from the Canadian Institutes of Health Research

awarded to A.J.R. This work was also supported, in part, by a grant from the JSPS Strategic Young Researcher Overseas Visits Program (awarded to R.K.), by NSERC Grant 298366-2009 to

A.G.B.S., by a Czech Science Foundation grant to I.Č. (project GA14-14105S) and by grants from the Japan Society for the Promotion of Science (JSPS; nos 15H05606 and 15K14591 awarded to

R.K., 23117005 and 15H05231 awarded to T.H., and 23117006 awarded to Y.I.). We thank A. A. Heiss for his help with _Trimastix marina_ data generation, and N. Ros for her comments on the

manuscript. AUTHOR INFORMATION Author notes * Michelle M. Leger, Martin Kolisko, Courtney W. Stairs & Laura Eme Present address: ‡ Present addresses: Institute of Evolutionary Biology,

CSIC-Universitat Pompeu Fabra, Passeig Marítim de la Barceloneta, 37–49, 08003 Barcelona, Spain (M.M.L.); Institute of Parasitology, Biology Centre, Czech Academy of Sciences, Branišovská

1160/31, 370 05 České Budĕjovice, Czech Republic (M.K.); Department of Cell and Molecular Biology, Uppsala University, Box 596, 751 24 Uppsala, Sweden (C.W.S. and L.E.), * Michelle M. Leger,

Martin Kolisko and Ryoma Kamikawa: These authors contributed equally to this work. AUTHORS AND AFFILIATIONS * Department of Biochemistry and Molecular Biology, Dalhousie University, 5850

College Street, PO Box 15000, Halifax, Nova Scotia, B3H 4R2, Canada Michelle M. Leger, Martin Kolisko, Courtney W. Stairs, Laura Eme & Andrew J. Roger * Graduate School of Human and

Environmental Studies, Graduate School of Global Environmental Studies, Kyoto University, Yoshida-Honmachi, Sakyo-ku, Kyoto, 606-8501, Japan Ryoma Kamikawa * Graduate School of Life and

Environmental Sciences, Center for Computational Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, 305-8572, Ibaraki, Japan Keitaro Kume, Yuji Inagaki & Tetsuo Hashimoto *

Department of Zoology, Faculty of Science, Charles University, Vinicna 7, 128 44, Prague 2, Czech Republic Ivan Čepička * Department of Biological Sciences, University of Arkansas,

Fayetteville, 72701, Arkansas, USA Jeffrey D. Silberman * Department of Cell and Molecular Biology, Uppsala University, Box 596, Uppsala, , 751 24, Sweden Jan O. Andersson & Feifei Xu *

Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15, Natsushima-cho, Yokosuka, 237-0061, Kanagawa, Japan Akinori Yabuki & Kiyotaka Takishita * Yantai Institute of

Coastal Zone Research, Chinese Academy of Sciences, 17 Chunhui Road, Yantai, 264003, Shandong, People’s Republic of China Qianqian Zhang * Center for Computational Sciences, University of

Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8577, Japan Yuji Inagaki & Tetsuo Hashimoto * Department of Biology, Dalhousie University, 1355 Oxford Street, PO Box 15000, Halifax, B3H

4R2, Nova Scotia, Canada Alastair G. B. Simpson Authors * Michelle M. Leger View author publications You can also search for this author inPubMed Google Scholar * Martin Kolisko View author

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Stairs View author publications You can also search for this author inPubMed Google Scholar * Keitaro Kume View author publications You can also search for this author inPubMed Google

Scholar * Ivan Čepička View author publications You can also search for this author inPubMed Google Scholar * Jeffrey D. Silberman View author publications You can also search for this

author inPubMed Google Scholar * Jan O. Andersson View author publications You can also search for this author inPubMed Google Scholar * Feifei Xu View author publications You can also

search for this author inPubMed Google Scholar * Akinori Yabuki View author publications You can also search for this author inPubMed Google Scholar * Laura Eme View author publications You

can also search for this author inPubMed Google Scholar * Qianqian Zhang View author publications You can also search for this author inPubMed Google Scholar * Kiyotaka Takishita View author

publications You can also search for this author inPubMed Google Scholar * Yuji Inagaki View author publications You can also search for this author inPubMed Google Scholar * Alastair G. B.

Simpson View author publications You can also search for this author inPubMed Google Scholar * Tetsuo Hashimoto View author publications You can also search for this author inPubMed Google

Scholar * Andrew J. Roger View author publications You can also search for this author inPubMed Google Scholar CONTRIBUTIONS M.K., R.K., J.O.A., Y.I., A.G.B.S., T.H. and A.J.R. conceived and

designed the experiments; M.K., K.K., I.Č., J.D.S., F.X., A.Y. and Q.Z. performed the experiments; M.M.L., M.K., R.K., C.W.S., K.K., L.E. and Y.I. analysed the data; R.K., C.W.S., J.D.S.,

K.T., Y.I., A.G.B.S., T.H. and A.J.R. contributed materials and/or analysis tools; and M.M.L., M.K., R.K., A.G.B.S. and A.J.R. wrote the paper. CORRESPONDING AUTHORS Correspondence to Tetsuo

Hashimoto or Andrew J. Roger. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing financial interests. SUPPLEMENTARY INFORMATION SUPPLEMENTARY INFORMATION Supplementary

Figures 1–20, Supplementary Table 1 (PDF 1444 kb) SUPPLEMENTARY DATA 1 Predicted mitochondrion-related organelle proteins, and selected predicted cytosolic proteins, in metamonads. (XLSX

149 kb) SUPPLEMENTARY DATA 2 File containing the raw phylogenetic trees depicted in Supplementary Figs 4–20, including bootstrap support values, in Newick format. (TXT 539 kb) RIGHTS AND

PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Leger, M., Kolisko, M., Kamikawa, R. _et al._ Organelles that illuminate the origins of _Trichomonas_ hydrogenosomes

and _Giardia_ mitosomes. _Nat Ecol Evol_ 1, 0092 (2017). https://doi.org/10.1038/s41559-017-0092 Download citation * Received: 17 August 2016 * Accepted: 17 January 2017 * Published: 13

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